Grouping of Spindle Activity during Slow Oscillations in Human Non-Rapid Eye Movement Sleep

Abstract

Based on findings primarily in cats, the grouping of spindle activity and fast brain oscillations by slow oscillations during slow-wave sleep (SWS) has been proposed to represent an essential feature in the processing of memories during sleep. We examined whether a comparable grouping of spindle and fast activity coinciding with slow oscillations can be found in human SWS. For negative and positive half-waves of slow oscillations (dominant frequency, 0.7-0.8 Hz) identified during SWS in humans (n = 13), wave-triggered averages of root mean square (rms) activity in the theta (4-8 Hz), alpha (8-12 Hz), spindle (12-15 Hz), and beta (15-25 Hz) range were formed. Slow positive half-waves were linked to a pronounced and microV (23.4%; p < 0.001, with reference to baseline) at the midline central electrode (Cz). In contrast, spindle activity was suppressed during slow negative half-waves, on average by -0.65 +/- 0.06 microV at Cz (-22%; p < 0.001). An increase in spindle activity 400-500 msec after negative half-waves was more than twofold the increase during slow positive half-waves (p < 0.001). A similar although less pronounced dynamic was observed for beta activity, but not for alpha and theta frequencies. Discrete spindles identified during stages 2 and 3 of non-rapid eye movement (REM) sleep coincided with a discrete slow positive half-wave-like potential preceded by a pronounced negative half-wave (p < 0.01). These results provide the first evidence in humans of grouping of spindle and beta activity during slow oscillations. They support the concept that phases of cortical depolarization during slow oscillations, reflected by surface-positive (depth-negative) field potentials, drive the thalamocortical spindle activity. The drive is particularly strong during cortical depolarization, expressed as surface-positive field potentials.

Interaction between neocortical and hippocampal networks via slow oscillations

“…6) (Isomura et al, 2006;Moelle et al, 2006). As discussed earlier, the DOWN-UP transition is a crucial state because it can trigger K complexes and sleep spindles (Amzica and Steriade, 1997;Massimini et al, 2004;Molle et al, 2002). The temporal association of hippocampal ripples and sleep spindles in the neocortex on the scale of ∼1 sec has led investigators to hypothesize that the hippocampal SPW output is responsible for the DOWN-UP shift and the occurrence of sleep spindles in neocortical networks (Siapas and Wilson, 1998;Battaglia et al, 2004).…”

“…They referred to the newly discovered rhythm as 'slow' oscillation because of its frequency between 0.5 and 1.5 Hz. Slow oscillation was soon shown also in the human EEG during sleep (Achermann and Borbely, 1997;Amzica and Steriade, 1997;Molle et al, 2002), indicating its crucial importance for neocortical function. An important aspect of slow oscillation is its ability to temporally organize other cortical patterns, such as sleep spindles, gamma oscillations and K complexes (Achermann and Borbely, 1997;Amzica and Steriade, 1997;Molle et al, 2002;Steriade and Amzica, 1998a;Mukovski et al, 2006) and hippocampal sharp wave ripples (Sirota et al, 2003).…”

“…Because slower oscillations affect larger neuronal populations, they often modulate the power of faster oscillatory events. Simply by changing the phase offset, the phase modulation mechanism can reverse instantaneously the direction of information transfer Steriade et al, 1996;Chrobak and Buzsáki, 1998b;Steriade and Amzica, 1998a;Molle et al, 2002;Sirota et al, 2003;Buzsáki and Draguhn, 2004;Siapas et al, 2005;Buzsáki, 2006). In the remainder of the review, we illustrate how the slow oscillations described by Steriade interact with various other rhythms across brain structures.…”

Sleep spindles are locally modulated by training on a brain–computer interface

“…Sleep spindles are one of the most prominent and recognizable of these oscillations, and as such they are commonly used to classify NREM sleep stages. These brief 12-to 15-Hz oscillations are generated by the reticular nucleus of the thalamus and grouped by the slow oscillation (<1 Hz) in the neocortex (3). The reticular nucleus is involved in gating sensory inputs and it is hypothesized that sleep spindles prevent incoming sensory information from reaching the neocortex during NREM sleep (4).…”

A neurophysiological perspective on sleep and its maturation

“…However, these changes do not appear as a linear process, but rather as a continuum of coalescing low and high frequency oscillations under the slow oscillation. 49 One EEG manifestation of the slow oscillation is the socalled 'cyclic alternating pattern' (CAP). This consists of transient arousal complexes (phase A) that periodically interrupt the tonic theta/delta activities of NREM sleep (phase B).…”